A transcriptional activator from Rhizophagus irregularis regulates phosphate uptake and homeostasis in AM symbiosis during phosphorous starvation

Abstract

IntroductionPhosphorus (P) is one of the most important nutrient elements for plant growth and development. Under P starvation, arbuscular mycorrhizal (AM) fungi can promote phosphate (Pi) uptake and homeostasis within host plants. However, the underlying mechanisms by which AM fungal symbiont regulates the AM symbiotic Pi acquisition from soil under P starvation are largely unknown. Here, we identify a HLH domain containing transcription factor RiPho4 from Rhizophagus irregularis.MethodsTo investigate the biological functions of the RiPho4, we combined the subcellular localization and Yeast One-Hybrid (Y1H) experiments in yeasts with gene expression and virus-induced gene silencing approach during AM symbiosis.ResultsThe approach during AM symbiosis. The results indicated that RiPho4 encodes a conserved transcription factor among different fungi and is induced during the in planta phase. The transcription of RiPho4 is significantly up-regulated by P starvation. The subcellular localization analysis revealed that RiPho4 is located in the nuclei of yeast cells during P starvation. Moreover, knock-down of RiPho4 inhibits the arbuscule development and mycorrhizal Pi uptake under low Pi conditions. Importantly, RiPho4 can positively regulate the downstream components of the phosphate (PHO) pathway in R. irregularis.DiscussionIn summary, these new findings reveal that RiPho4 acts as a transcriptional activator in AM fungus to maintain arbuscule development and regulate Pi uptake and homeostasis in the AM symbiosis during Pi starvation.

Short-term artificial adaptation of Rhizoglomus irregulare to high phosphate levels and its implications for fungal-plant interactions: phenotypic and transcriptomic insights

“…The histochemical staining of alkaline phosphatase is considered to be a marker of polyphosphate metabolic activity localized in fungal tissues within the roots, and usually coincides with plant growth stimulation. It is also known that the intensity of alkaline phosphatase decreases with the age of colonization or when soluble phosphate is added to the substrate, and that this metabolic activity is associated with mycorrhizal functionality and ability to transfer phosphate to the plant ( Tisserant et al., 1993 ; Vivas et al., 2003 ; Aono et al., 2004 ; Funamoto et al., 2007 ; Zhang et al., 2023 ). Our data are partially consistent with these previous observations when comparing both fungal phenotypes under low Pi.…”

“… Xie et al. (2016) and Zhang et al. (2023) reported that PT1 was repressed by Pi in Gigapora margarita and R. irregulare , whereas Fiorilli et al.…”

“…In fungi, at least 9 PT isoforms have been characterized in R. irregulare , expressed in both intra- and extra-radical mycelium ( Benedetto et al., 2005 ; Balestrini et al., 2007 ; Tisserant et al., 2012 ; Fiorilli et al., 2013 ; Walder et al., 2016 ; Mercy et al., 2017 ; Zhou et al., 2021 ; Xie et al., 2022 ). Furthermore, the fungal phosphate homeostasis is regulated by the PHO pathway, and the recent expansion of sequenced Glomeromycota genomes has revealed that AMF possess many key genes involved in this pathway ( Tisserant et al., 2012 ; Zhou et al., 2021 ), some of which have been shown to be significantly regulated in mycorrhizal roots in response to phosphate ( Zhou et al., 2021 ; Zhang et al., 2023 ). From the plant side, host plants possess two possible Pi uptake routes: the direct uptake pathway (DUP), mediated by non-mycorrhiza-regulated Pht1 members, and the mycorrhizal uptake pathway (MUP), facilitated by AM-induced or AM-specific PTs ( Bucher, 2007 ; Javot et al., 2007 ; Ferrol et al., 2019 ).…”

Spatial co-transcriptomics reveals discrete stages of the arbuscular mycorrhizal symbiosis

“…Recent advances in CRISPR-Cas9 89 gene editing and continued efforts in creating pure cultures of AM fungi 18 , 19 will hopefully bring forth a new chapter of AM symbiotic research that focuses on the fungal partner. Recent efforts in improving AM fungal genome assemblies 90 , 91 and functional characterization of R. irregularis genes involved in symbiosis 69 , 77 – 79 , 92 , 93 lay the groundwork for this shift. We identified spatial cluster 3 as AM-responsive based on the expression of both M. truncatula and R. irregularis marker genes for the AM symbiosis.…”

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“…However, under unfavourable conditions, mycorrhizal fungi compete with plants for food elements and become consumers instead of a source(Kokkoris et al, 2019). Thus, mycorrhizal fungi can reabsorb phosphorus released on the periarbuscular surface and control its supply to the partner plant(Kokkoris et al, 2019;Zhang et al, 2023).…”